Lack of strong innate immune reactivity renders macrophages alone unable to control productive Varicella-Zoster Virus infection in an isogenic human iPSC-derived neuronal co-culture model

Front Immunol. 2023 May 23:14:1177245. doi: 10.3389/fimmu.2023.1177245. eCollection 2023.

Abstract

With Varicella-Zoster Virus (VZV) being an exclusive human pathogen, human induced pluripotent stem cell (hiPSC)-derived neural cell culture models are an emerging tool to investigate VZV neuro-immune interactions. Using a compartmentalized hiPSC-derived neuronal model allowing axonal VZV infection, we previously demonstrated that paracrine interferon (IFN)-α2 signalling is required to activate a broad spectrum of interferon-stimulated genes able to counteract a productive VZV infection in hiPSC-neurons. In this new study, we now investigated whether innate immune signalling by VZV-challenged macrophages was able to orchestrate an antiviral immune response in VZV-infected hiPSC-neurons. In order to establish an isogenic hiPSC-neuron/hiPSC-macrophage co-culture model, hiPSC-macrophages were generated and characterised for phenotype, gene expression, cytokine production and phagocytic capacity. Even though immunological competence of hiPSC-macrophages was shown following stimulation with the poly(dA:dT) or treatment with IFN-α2, hiPSC-macrophages in co-culture with VZV-infected hiPSC-neurons were unable to mount an antiviral immune response capable of suppressing a productive neuronal VZV infection. Subsequently, a comprehensive RNA-Seq analysis confirmed the lack of strong immune responsiveness by hiPSC-neurons and hiPSC-macrophages upon, respectively, VZV infection or challenge. This may suggest the need of other cell types, like T-cells or other innate immune cells, to (co-)orchestrate an efficient antiviral immune response against VZV-infected neurons.

Keywords: RNA-seq analysis; axonal infection; iPSC; innate immune response; macrophages; neuronal models; neurons; varicella zoster virus.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antiviral Agents
  • Chickenpox*
  • Coculture Techniques
  • Herpes Zoster*
  • Herpesvirus 3, Human
  • Humans
  • Immunity, Innate
  • Induced Pluripotent Stem Cells*
  • Interferons
  • Macrophages
  • Neurons
  • Varicella Zoster Virus Infection*
  • Virus Replication / physiology

Substances

  • Interferons
  • Antiviral Agents

Grants and funding

This research was funded by the Fund for Scientific Research Flanders (FWO-Vlaanderen) (G067118N granted to KL, PD, and BO; G091518N granted to PP, 1861219N granted to BO and G034721N granted to PP, PD, BO, ML, and CS-D), the Industrial Research Fund (IOF, IOF-SBO 2018 granted to PP) and the ‘Bijzonder Onderzoeksfonds’ (BOF, BOF-GOA 2020 granted to PP) of the University of Antwerp. EB and TB-H are holders of a PhD fellowship that is provided by the University of Antwerp (DOCPRO mandates 36946 and 34720). JS received a PhD fellowship from the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement No 813263.